Posttranscriptional coordination of splicing and miRNA biogenesis in plants

Advanced Review

Agata Stepien, Katarzyna Knop, Jakub Dolata, Michal Taube, Mateusz Bajczyk, Maria Barciszewska‐Pacak, Andrzej Pacak, Artur Jarmolowski, Zofia Szweykowska‐Kulinska

Published Online: Nov 09 2016

DOI: 10.1002/wrna.1403

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MicroRNAs (miRNAs) are short, single‐stranded, noncoding RNAs that play a crucial role in basic physiological and morphological processes and in response to various stresses in eukaryotic organisms. However, the miRNA biogenesis, which is based on the action of complex protein machinery, varies between plants and animals, with the differences largely concerning the location of the process, the protein composition of the microprocessor, the mechanism of miRNA action on mRNA target, and the miRNA gene (MIR) structure. Roughly half of known Arabidopsis MIRs contain introns, and 29 miRNAs are encoded within the introns of host genes. Selection of alternative transcription start sites, alternative splice sites (SSs), and polyadenylation sites has been identified within miRNA primary transcripts (pri‐miRNAs), and such variety is essential for the production and fine‐tuning of miRNA levels. For example, the posttranscriptional processing of intron‐containing pri‐miRNAs involves the action of additional RNA metabolism machineries, such as the spliceosome and polyadenylation machinery, and to a large extent is based on direct communication between SERRATE (one of the core components of the plant microprocessor) and U1 snRNP auxiliary proteins. Moreover, the position of the miRNA stem–loop structure relative to the closest active 5′SS is essential for the miRNA production efficiency. Indeed, it is highly probable that this pre‐miRNA location affects recruitment of the microprocessor to pri‐miRNAs and therefore influences miRNA maturation and target mRNA regulation. Such complicated crosstalk between several machineries is important for a proper miRNA‐connected response to biotic and abiotic stresses, ensuring plant survival in a changing environment. WIREs RNA 2017, 8:e1403. doi: 10.1002/wrna.1403 This article is categorized under: RNA Evolution and Genomics > RNA and Ribonucleoprotein Evolution

Comparison of microRNA (miRNA) production and activity pathways in plants and humans. In plants, miRNA/miRNA* duplexes are cleaved from pri‐miRNA precursors in two steps. First, pre‐miRNAs are produced by DCL1 endonuclease, which is accompanied by other microprocessor proteins; DCL1 then excises mature miRNA/miRNA* duplexes, and the 2′‐OH groups on the 3′ terminal nucleotides are methylated. These processes occur in the nucleus. In contrast, human pre‐miRNAs are produced in the nucleus by the action of the Drosha enzyme, DGCR8 protein (also known as Pasha in Caenorhabditis elegans), and other proteins. Duplexes of miRNA/miRNA* are further processed from pre‐miRNAs in the cytoplasm by Dicer. In plants, miRNA/miRNA* duplexes are transported from the nucleus to the cytoplasm by the HASTY protein, whereas the Exportin 5 (XPO5) protein is involved in pre‐miRNA precursor transport from the nucleus to the cytoplasm in humans. Ten AGO proteins exist in Arabidopsis, at least eight of which can recruit different classes of small RNAs. In addition to cleavage activity, the Arabidopsis AGO1 protein (the most important protein in the miRNA pathway) is also associated with polysomes and represses translation. Humans have four AGOs, but only AGO2 possesses cleavage activity. The presence of the cap‐binding motif in the human AGO2 protein also enables the repression of translation initiation by precluding the recruitment of factor eIF4E. The red and blue lines represent miRNA and miRNA* molecules, respectively. Arrows indicate the direction of the subsequent biogenesis steps. All protein abbreviations are listed in Table .

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Proposed model of the crosstalk between the microprocessor, 5′ splice site (5′SS), and U1 snRNP that is essential for proper biogenesis of miRNAs derived from intron‐containing precursors. Direct communication between the microprocessor and the spliceosome is responsible for exonic and intronic miRNA maturation efficiency. Moreover, the position of the miRNA stem–loop structure with regard to the closest 5′SS is pivotal for the recruitment order of these machineries to the miRNA precursor. First, cap‐binding complex (CBC) binds to the cap structure of the pri‐miRNA or miRNA‐hosting pre‐mRNA. (a) Next, for exonic miRNAs, the core microprocessor (DCL1, HYL1, and SE) recognizes the pre‐miRNA hairpin. Then, U1 snRNP binds to the downstream active 5′SS. This stabilizes the microprocessor–spliceosome association (via direct SE–U1 snRNP auxiliary protein interactions), resulting in effective miRNA biogenesis. (b) For intronic miRNAs, the 5′SS of the miRNA‐carrying intron, located upstream of the pre‐miRNA hairpin, is recognized by U1 snRNP; SE is then recruited. This U1 snRNP–SE interaction enhances the splicing efficiency of the miRNA‐hosting intron and impairs intronic miRNA maturation by making SERRATE less available to other proteins of the microprocessor (located downstream of the miRNA stem–loop structure).

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Pri‐miRNA and pre‐mRNA processing complexes share the same factors. RNA polymerase II (RNA Pol II) transcripts of microRNA (miRNA)‐coding genes as well as protein‐coding genes are capped at the 5′ end. In both cases, the cap‐binding complexes, which consist of the subunits CBP20 and CBP80, interact with the SE protein. All these proteins are involved in pri‐miRNA processing and pre‐mRNA splicing.

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Heat‐stress‐induced splicing inhibition of microRNA (miRNA)‐carrying introns stimulates the production of mature miR402, which is involved in regulating DNA demethylase (DML3) expression levels. Left pathway: Efficient splicing of the At1g77230 first intron and preferential selection of the distal polyA site correlate with a low level of mature miR402 and high accumulation of the host‐gene mRNA. The proper expression level of miR402 target mRNA, DML3 (Demeter Like Protein 3, At4g34060), is required to maintain a low level of DNA methylation. Right pathway: Under heat stress conditions, splicing of the miR402‐carrying intron is less efficient, and the proximal intronic polyA site selection is preferred, leading to increases in the level of mature miR402 and downregulation of the host‐mRNA level. Therefore, the level of DML3 mRNA decreases, and DNA methylation increases. Dark and light gray boxes represent exons and UTRs, respectively, and horizontal black lines depict introns; vertical lines denote polyA sites. Red and blue boxes within the MIR structure represent miRNA and miRNA* molecules, respectively, as with the red and blue parts of the pre‐miRNA hairpin. Broken red lines indicate the miRNA cleavage site within the target mRNA. Red and green arrows represent downregulation and upregulation of the levels of target mRNA expression and DNA methylation, respectively.

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Regulation of the biogenesis of miR163, which is involved in proper plant responses to biotic stress. Splicing of pri‐miR163 stimulates the biogenesis of mature microRNA (miRNA), leading to a higher rate of cleavage of its target mRNA (S‐adenosyl‐l‐methionine‐dependent methyltransferase, At1g66690). An accurate methyltransferase mRNA level is required for the proper response of Arabidopsis to Pseudomonas syringae infection. Bacterial‐triggered induction of miR163 depends on a functional 5′ splice site (5′SS, left pathway) because its inactivation, accompanied by higher intronic proximal polyA site selection, results in lower efficiency of miR163 maturation and upregulation of levels of methyltransferase mRNA (right pathway). Gray boxes represent exons; horizontal black lines depict introns, and vertical lines denote polyA sites. Red and blue boxes within the MIR structure represent miRNA and miRNA* molecules, respectively, as with the red and blue parts of the pre‐miRNA hairpin. Broken red lines indicate the miRNA cleavage site within the target mRNA. Red and green arrows represent downregulation and upregulation of the level of target mRNA expression, respectively.

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Regulation of microRNA (miRNA) precursor levels produced from MIR842/846 upon application of exogenous abscisic acid (ABA). In Arabidopsis, miR842 and miR846 arise from different alternatively spliced products. miR846 is expressed from pri‐miR846 (isoform 1), whereas miR842 arises from pri‐miR842 (isoform 2) and potentially from the intron produced during the splicing of isoforms 1 and 3. Exogenous application of ABA to seedlings mediates these alternative splicing (AS) events by reducing the levels of functional isoform 1 and increasing those of nonfunctional isoform 3 but not changing the levels of isoform 2. Dark gray boxes represent constitutive exons of particular pri‐miRNA isoform. White boxes denote AS‐spliced exons of particular pri‐miRNA isoform. Horizontal black lines represent introns. Pre‐miRNA842 and pre‐miRNA846 are shown by the miRNA stem–loop structures containing miRNA/miRNA* duplexes (miRNA in red, miRNA* in blue). Broken black lines indicate AS events. The 5′ splice site (5′SS) and 3′ splice site (3′SS) at the boundaries of introns are shown. Arrows and an equal sign show the changes in isoform expression upon ABA application.

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Gene structures and complex processing of pri‐miRNAs in Arabidopsis. (a) The majority of Arabidopsis miRNA genes are transcribed as independent transcription units, which can be intronless (28 genes) or possess introns (27 genes). In the case of intron‐containing precursors, the microRNA (miRNA) stem–loop structure is found mainly within the first exon. Plant miRNAs are also encoded within the transcripts of protein‐coding and noncoding genes (27 genes). Within MIRs with known structure, four genes can be transcribed as polycistronic transcription units. (b) Intron‐containing pri‐miRNAs exhibit complicated constitutive and alternative splicing (AS) patterns, which can lead to intron retention and/or exon skipping. In many cases, selection of an alternative 5′ splice site (5′SS) and/or 3′ splice site (3′SS) results in the generation of transcripts with altered exon or intron lengths. AS events can lead to changes in the level of mature miRNAs and may potentially regulate miRNA gene expression. Examples of alternatively spliced transcripts of the MIR172b and MIR156c genes are presented in box b. (c) Many alternative polyadenylation sites are present in plant pri‐miRNAs. In many cases, selection of these sites under various conditions leads to the production of pri‐miRNAs of different lengths, such as for MIR399d precursors. All presented gene structures and pri‐miRNA isoforms are derived from the mirEX 2.0 database.

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